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Period of susceptibility of almonds to aflatoxin contamination during development in the orchard

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Abstract

Almonds can be contaminated with aflatoxins, produced mainly by Aspergillus flavus and A. parasiticus. Infection can be facilitated by insect injuries during hull split, which begins four to six weeks before harvest. Within this period, it is unknown which kernel stages are most susceptible to aflatoxin contamination. Developing almonds of the Nonpareil cultivar were inoculated weekly with a spore suspension of A. flavus or A. parasiticus for five weeks after hull split in 2013. The almonds were infested with eggs of the lepidopteron navel orangeworm (NOW) (Amyelois transitella) before each spore inoculation. Aflatoxin levels were quantified at harvest using HPLC. Aflatoxin contamination was consistently higher in NOW-damaged kernels, although aflatoxins were also detected in undamaged kernels at each inoculation date. Insect injury is not required for kernel infection but it is a key risk factor for high aflatoxin contamination. Laboratory inoculations were also performed on Nonpareil almond kernels collected during the summers of 2013 and 2015. Aflatoxin levels were significantly lower on dried almonds but the ability to produce aflatoxins was restored when almonds were incubated with high humidity or when the Aspergillus species were inoculated on almond meal agar amended with ground kernels. Therefore, aflatoxins can accumulate in kernels with low aw, should sufficient moisture favors aflatoxin production. In our field experiment, the orchard micro-climate had sufficient humidity to enable aflatoxin production in both damaged and undamaged dried kernels.

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References

  • Almond Board of California. (2013). 2013 Almond almanac. Resource document. http://www.almondboard.com/AboutTheAlmondBoard/Documents/2013%20Almanac%20-%20Final.pdf. Accessed 30 May 2016.

  • Ampt, E. A., Bush, D. S., Siegel, J. P., & Berenbaum, M. R. (2016). Larval preference and performance of Amyelois transitella (navel orangeworm, Lepidoptera: Pyralidae) in relation to the fungus Aspergillus flavus. Environmental Entomology, 45, 155–162.

    Article  PubMed  Google Scholar 

  • AOAC Official Method 991.31. (2000). Aflatoxins in corn, raw peanuts and peanut butter: immunoaffinity column (AflaTest) Method. AOAC International, p. 49.2.18.

  • Arrus, K., Blank, G., Abramson, D., Clear, R., & Holley, R. A. (2005). Aflatoxin production by Aspergillus flavus in Brazil nuts. Journal of Stored Products Research, 41, 513–527.

    Article  CAS  Google Scholar 

  • Astoreca, A., Vaamonde, G., Dalcero, A., Marín, S., & Ramos, A. (2014). Abiotic factors and their interactions influence on the co-production of aflatoxin B1 and cyclopiazonic acid by aspergillus flavus isolated from corn. Food Microbiology, 38, 267–283.

    Article  Google Scholar 

  • Campbell, B. C., Molyneux, R. J., & Schatzki, T. F. (2003). Current research on reducing pre-and post-harvest aflatoxin contamination of US almond, pistachio, and walnut. Toxin Reviews, 22, 225–266.

    CAS  Google Scholar 

  • Cotty, P. J. (1989). Virulence and cultural characteristics of two Aspergillus flavus strains pathogenic on cotton. Phytopathology, 79, 808–814.

    Article  Google Scholar 

  • Cotty, P. J., & Jaime-Garcia, R. (2007). Influences of climate on aflatoxin producing fungi and aflatoxin contamination. International Journal of Food Microbiology, 119, 109–115.

    Article  CAS  PubMed  Google Scholar 

  • Curtis, R. K., & Barnes, M. (1977). Oviposition and development of the navel orangeworm in relation to almond maturation. Journal of Economic Entomology, 70, 395–398.

    Article  Google Scholar 

  • Donner, M., Lichtemberg, P. S. F., Doster, M., Picot, A., Cotty, P. J., Puckett, R., & Michailides, T. J. (2015). Community structure of Aspergillus flavus and A. parasiticus in major almond-producing areas of California, United States. Plant Disease, 99, 1161–1169.

    Article  Google Scholar 

  • Doster, M. A., & Michailides, T. J. (1994). Development of Aspergillus molds in litter from pistachio trees. Plant Disease, 78, 393–397.

    Article  Google Scholar 

  • Food and Drug Administration. (1994). Manual of compliance policy guides (Sec. 683.100 Action Levels for Aflatoxins in Animal Feeds). Washington DC: Office of Regulatory Affairs.

  • Food and Drug Administration. (2005). Manual of compliance policy guides (Sec. 570.375 Aflatoxin in Peanuts and Peanut Products). Washington DC: Office of Regulatory Affairs.

  • Gallo, A., Solfrizzo, M., Epifani, F., Panzarini, G., & Perrone, G. (2016). Effect of temperature and water activity on gene expression and aflatoxin biosynthesis in Aspergillus flavus on almond medium. International Journal of Food Microbiology, 217, 162–169.

    Article  CAS  PubMed  Google Scholar 

  • Giorni, P., Magan, N., Pietri, A., & Battilani, P. (2011). Growth and aflatoxin production of an Italian strain of Aspergillus flavus: influence of ecological factors and nutritional substrates. World Mycotoxin Journal, 4, 425–432.

    Article  CAS  Google Scholar 

  • Gradziel, T., & Kester, D. E. (1994). Breeding for resistance to Aspergillus flavus in almond. Acta Horticulturae, 373, 111–118.

    Article  Google Scholar 

  • Gradziel, T., Mahoney, N., & Abdallah, A. (2000). Aflatoxin production among almond genotypes is not related to either kernel oil composition or Aspergillus flavus growth rate. Hortscience, 35, 937–939.

    CAS  Google Scholar 

  • International Agency for Research on Cancer, Aflatoxins (Group 1). (2002). In IARC monographs on the evaluation of carcinogenic risks to humans volume 82: some traditional herbal medicines, some mycotoxins, naphthalene and styrene. Resource document. https://monographs.iarc.fr/ENG/Monographs/vol82/mono82.pdf. Accessed 30 May 2016.

  • Keller, N. P., Nesbitt, C., Sarr, B., Phillips, T. D., & Burow, G. B. (1997). pH regulation of sterigmatocystin and aflatoxin biosynthesis in Aspergillus spp. Phytopathology, 87, 643–648.

    Article  CAS  PubMed  Google Scholar 

  • King Jr., A. D., Halbrook, W. U., Fuller, G., & Whiteland, L. C. (1983). Almond nutmeat moisture and water activity and its influence on fungal flora and seed composition. Journal of Food Science, 48, 615–617.

    Article  Google Scholar 

  • Klich, M. A. (2007). Aspergillus flavus: the major producer of aflatoxin. Molecular Plant Pathology, 8, 713–722.

    Article  CAS  PubMed  Google Scholar 

  • Mahoney, N., Molyneux, R. J., McKenna, J., Leslie, C. A., & McGranahan, G. (2003). Resistance of ‘Tulare’ walnut (Juglans regia cv. Tulare) to aflatoxigenesis. Journal of Food Science, 68, 619–622.

    Article  CAS  Google Scholar 

  • Mateles, R. I., & Adye, J. C. (1965). Production of aflatoxins in submerged culture. Applied Microbiology, 13, 208–211.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Molina, M., & Giannuzzi, L. (2002). Modelling of aflatoxin production by Aspergillus parasiticus in a solid medium at different temperatures, pH and propionic acid concentrations. Food Research International, 35, 585–594.

    Article  CAS  Google Scholar 

  • Molyneux, R. J., Mahoney, N., Kim, J. H., & Campbell, B. C. (2007). Mycotoxins in edible tree nuts. International Journal of Food Microbiology, 119, 72–78.

    Article  CAS  PubMed  Google Scholar 

  • Ozay, G., Seyhan, F., Pembeci, C., Saklar, S., & Yilmaz, A. (2007). Factors influencing fungal and aflatoxin levels in Turkish hazelnuts (Corylus avellana L.) during growth, harvest, drying and storage: a 3-year study. Food Additive and Contaminants Part A Chemistry, Analysis, Control, Exposure & Risk Assessment, 25, 209–218.

    Google Scholar 

  • Palumbo, J. D., Mahoney, N. E., & Light, D. M. (2008). Navel orangeworm (Amyelois transitella) as a vector of Aspergillus flavus on almonds. Phytopathology, 98, S119.

    Google Scholar 

  • Palumbo, J. D., Mahoney, N. E., Light, D. M., Siegel, J., Puckett, R. P., & Michailides, T. J. (2014). Spread of Aspergillus flavus by navel orangeworm (Amyelois transitella) on almonds. Plant Disease, 98, 1194–1199.

    Article  Google Scholar 

  • Picot, A., Barreau, C., Pinson-Gadais, L., Caron, D., Lannou, C., & Richard-Forget, F. (2011). The dent stage of maize kernels is the most conducive for fumonisin biosynthesis under field conditions. Applied and Environmental Microbiology, 77, 8382–8390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rapid Alert System for Food and Feed (RASFF). (2016). Annual Report 2015. Publication Office of the European Union, European Commission, Luxembourg. https://webgate.ec.europa.eu/rasff-window/portal/?event=SearchForm&cleanSearch=1. RASFF Portal Accessed September 20 2016.

  • Sanchis, V., & Magan, N. (2004). Environmental profiles for growth and mycotoxin production. In N. Magan & M. Olsen (Eds.), Mycotoxins in Food: Detection and Control (pp. 174–189). Woodhead Publishing Ltd.

  • Schade, J. E., McGreevy, K., King, A. D. J., Mackey, B., & Fuller, G. (1975). Incidence of aflatoxin in California almonds. Applied Microbiology, 29, 48–53.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schatzki, T. F., & Ong, M. S. (2000). Distribution of aflatoxin in almonds. 2. Distribution in almonds with heavy insect damage. Journal of Agricultural and Food Chemistry, 48, 489–492.

    Article  CAS  PubMed  Google Scholar 

  • Schatzki, T. F., & Ong, M. S. (2001). Dependence of aflatoxin in almonds on the type and amount of insect damage. Journal of Agricultural and Food Chemistry, 49, 4513–4519.

    Article  CAS  PubMed  Google Scholar 

  • Siegel, J. P., Kuenen, L. P. S., & Ledbetter, C. (2010). Variable development rate and survival of navel orangeworm (Amyelois transitella, Lepidoptera: Pyralidae) on wheat bran diet and almonds. Journal of Economic Entomology, 103, 1250–1257.

    Article  PubMed  Google Scholar 

  • Taitano, L. Z., & Singh, R. P. (2013). Predictive modeling of textural quality of almonds during commercial storage and distribution. In S. Yanniotis, P. Taoukis, N. Stoforos, & V. T. Karathanos (Eds.), Advances in food process engineering research and applications, food engineering series (pp. 521–545). US: Springer.

    Chapter  Google Scholar 

  • Taitano, L. Z., Singh, R. P., Lee, J. H., & Kong, F. (2012). Thermodynamic analysis of moisture adsorption isotherms of raw and blanched almonds. Journal of Food Process Engineering, 35, 840–850.

    Article  CAS  Google Scholar 

  • Warfield, C. Y., & Gilchrist, D. G. (1999). Influence of kernel age on fumonisin B1 production in maize by Fusarium moniliforme. Applied and Environmental Microbiology, 65, 2853–2856.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitaker, T. B., Slate, A., Birmingham, T., Adams, J., Jacobs, M., & Gray, G. J. (2010). Correlation between aflatoxin contamination and various USDA grade categories of shelled almonds. Journal of AOAC International, 93, 943–947.

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are very grateful to Patricia Noble for providing NOW eggs and to Michael Luna for his help in the field experiments. UC Davis and USDA/ARS are equal opportunity employers.

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Correspondence to Themis J. Michailides.

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Picot, A., Ortega-Beltran, A., Puckett, R.D. et al. Period of susceptibility of almonds to aflatoxin contamination during development in the orchard. Eur J Plant Pathol 148, 521–531 (2017). https://doi.org/10.1007/s10658-016-1108-2

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  • DOI: https://doi.org/10.1007/s10658-016-1108-2

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